Large variations in bacterial ribosomal RNA genes - PubMed (original) (raw)

Large variations in bacterial ribosomal RNA genes

Kyungtaek Lim et al. Mol Biol Evol. 2012 Oct.

Abstract

Ribosomal RNA (rRNA) genes, essential to all forms of life, have been viewed as highly conserved and evolutionarily stable, partly because very little is known about their natural variations. Here, we explored large-scale variations of rRNA genes through bioinformatic analyses of available complete bacterial genomic sequences with an emphasis on formation mechanisms and biological significance. Interestingly, we found bacterial genomes in which no 16S rRNA genes harbor the conserved core of the anti-Shine-Dalgarno sequence (5'-CCTCC-3'). This loss was accompanied by elimination of Shine-Dalgarno-like sequences upstream of their protein-coding genes. Those genomes belong to 1 or 2 of the following categories: primary symbionts, hemotropic Mycoplasma, and Flavobacteria. We also found many rearranged rRNA genes and reconstructed their history. Conjecturing the underlying mechanisms, such as inversion, partial duplication, transposon insertion, deletion, and substitution, we were able to infer their biological significance, such as co-orientation of rRNA transcription and chromosomal replication, lateral transfer of rRNA gene segments, and spread of rRNA genes with an apparent structural defect through gene conversion. These results open the way to understanding dynamic evolutionary changes of rRNA genes and the translational machinery.

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Figures

F<sc>ig.</sc> 1.

Fig. 1.

Interaction between SD and anti-SD sequences. Interaction is between the mRNA 5′-UTR (for rpsB gene) and the 16S rRNA 3′ tail in Escherichia coli.

F<sc>ig.</sc> 2.

Fig. 2.

Comparative analysis of the anti-SD genomes and the non–anti-SD genomes in the class Flavobacteria. (A) Maximum likelihood phylogenetic tree. Groups 1 and 2 non-anti-SD genomes are shown in gray. (B) Predicted 16S rRNA 3′ tail sequences. The regions corresponding to the Escherichia coli anti-SD motif are shaded in gray. (C) SD indexes (d_F_SD). Triangle: cutoff value < −3.4535 kcal/mol; Dot: cutoff value < −4.4 kcal/mol. (D) Fractions of the four nucleotides (d_f_A, d_f_C, d_f_G, and d_f_T) at specific positions between −50 and −1 nt from all protein-coding genes in each genome. The background fraction was subtracted. For details, see Materials and Methods.

F<sc>ig.</sc> 3.

Fig. 3.

Comparative analysis of the anti-SD genomes and the non-anti-SD genomes in the phylum Proteobacteria. (A) Maximum likelihood phylogenetic tree. Group 3 non–anti-SD genomes are shown in gray. (B) Predicted 16S rRNA 3′ tail sequences. The regions corresponding to the Escherichia coli anti-SD motif are shaded in gray. (C) SD indexes (d_F_SD). Triangle: cutoff value < −3.4535 kcal/mol; Dot: cutoff value < −4.4 kcal/mol. (D) Fractions of the four nucleotides (d_f_A, d_f_C, d_f_G, and d_f_T) at specific positions between −50 and −1 nt from all protein-coding genes in each genome. The background fraction was subtracted. For details, see Materials and Methods. (i) The class Gammaproteobacteria. (ii) The class Betaproteobacteria. (iii) The class Alphaproteobacteria.

F<sc>ig.</sc> 4.

Fig. 4.

Comparative analysis of the anti-SD genomes and the non–anti-SD genomes in the genus Mycoplasma. (A) Maximum likelihood phylogenetic tree. Group 4 non–anti-SD genomes are shown in gray. (B) Predicted 16S rRNA 3′ tail sequences. The regions corresponding to the Escherichia coli anti-SD motif are shaded in gray. (C) SD indexes (d_F_SD). Triangle: cutoff value < −3.4535 kcal/mol; Dot: cutoff value < −4.4 kcal/mol. (D) Fractions of the four nucleotides (d_f_A, d_f_C, d_f_G, and d_f_T) at specific positions between −50 and −1 nt from all protein-coding genes in each genome. The background fraction was subtracted. For details, see Materials and Methods.

F<sc>ig.</sc> 5.

Fig. 5.

Inversion of rRNA operons. (A) Dotplot between genomes. (B) Reconstruction. (C) Recombination sites in one operon. (D) Recombination sites in the other operon. Amino acid names indicate the corresponding tRNA genes.

F<sc>ig.</sc> 6.

Fig. 6.

Partial duplication of rRNA genes. (A) Gene rearrangement in Actinobacillus pleuropneumoniae L20. (i) A proposed mechanism for the rearrangement: insertion with long target duplication. (ii) The other mechanism: tandem duplication followed by homologous recombination. (iii) The rearrangement. (B) Gene rearrangement in Bacillus thuringiensis BMB171. (i) A proposed mechanism for the rearrangement. (ii) The rearrangement.

F<sc>ig.</sc> 7.

Fig. 7.

An incomplete 16S rRNA gene on a plasmid. (A) Reconstruction. (B) The rearrangement. Two diverged regions between the two genes are boxed. (C) Sequence comparison in the diverged regions.

F<sc>ig.</sc> 8.

Fig. 8.

Transposon insertion. (A) An insertion into a 16S rRNA gene. (B) Another insertion into a 16S rRNA gene. Black arrows: target duplication. Gray arrows: incomplete inverted repeats at the transposon ends.

F<sc>ig.</sc> 9.

Fig. 9.

Other modes of rRNA gene rearrangements. (A) Internal deletion in a 16S rRNA gene. (B) Deletion in an rRNA operon. (C) Substitution. An amino acid name indicates the corresponding tRNA gene. (D) Inversion within an rRNA operon.

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References

    1. Acinas SG, Marcelino LA, Klepac-Ceraj V, Polz MF. Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J Bacteriol. 2004;186:2629–2635. - PMC - PubMed
    1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–410. - PubMed
    1. Barker EN, Helps CR, Peters IR, Darby AC, Radford AD, Tasker S. Complete genome sequence of Mycoplasma haemofelis, a hemotropic mycoplasma. J Bacteriol. 2011;193:2060–2061. - PMC - PubMed
    1. Boni IV, Isaeva DM, Musychenko ML, Tzareva NV. Ribosome-messenger recognition: mRNA target sites for ribosomal protein S1. Nucleic Acids Res. 1991;19:155–162. - PMC - PubMed
    1. Chang B, Halgamuge S, Tang SL. Analysis of SD sequences in completed microbial genomes: non-SD-led genes are as common as SD-led genes. Gene. 2006;373:90–99. - PubMed

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